Fibrous cap formation or destruction - The critical importance of vascular smooth muscle cell proliferation, migration and matrix formation

Cardiovascular Research

Volumn 41, Issue 2, 1999, Pages 345-360

  Newby, Andrew C ^a   Zaltsman, Alla B ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Arteriosclerosis; Extracellular matrix; Metalloproteinases; Vascular smooth muscle

Indexed keywords

METALLOPROTEINASE;

APOPTOSIS; ATHEROGENESIS; ATHEROSCLEROTIC PLAQUE; BASEMENT MEMBRANE; CELL AGING; CELL MIGRATION; CELL PROLIFERATION; CORONARY ARTERY THROMBOSIS; EXTRACELLULAR MATRIX; FOAM CELL; HUMAN; HUMAN TISSUE; MONOCYTE; PHENOTYPE; PRIORITY JOURNAL; REVIEW; SMOOTH MUSCLE FIBER; VASCULAR ENDOTHELIUM;

ANIMALS; APOPTOSIS; ARTERIOSCLEROSIS; CELL DIVISION; CELL MOVEMENT; ENDOTHELIUM, VASCULAR; EXTRACELLULAR MATRIX; GROWTH SUBSTANCES; HUMANS; LIPOPROTEINS, LDL; MACROPHAGES; METALLOENDOPEPTIDASES; MUSCLE, SMOOTH, VASCULAR;

EID: 0033026854     PISSN: 00086363     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0008-6363(98)00286-7     Document Type: Review

References (221)

1. Davies M., Richardson P., Woolf N., Katz D.R., Mann J. Risk of thrombosis in human atherosclerotic plaques: Role of extracellular lipid, macrophage and smooth muscle cell content. Br Heart J. 69:1993;377-381.
2. Falk E, Shah P, Fuster V. Pathogenesis of plaque rupture. In: Fuster V, Ross R, Topol E, editors. Atherosclerosis and coronary artery disease. Philadelphia, New York: Lippincott-Raven, 1996:491-500.
3. Shah P. Pathophysiology of plaque rupture and the concept of plaque stabilization. Cardiol Clin. 14:1996;17-29.
4. Lee R., Libby P. The unstable atheroma. Arterioscler Thromb Vasc Biol. 17:1997;1859-1867.
5. Ross R. The pathogenesis of atherosclerosis: a perspective for the 1990s. Nature. 362:1993;801-809.
6. Ross R., Glomset J.A. Atherosclerosis and the arterial smooth muscle cell. Proliferation of smooth muscle is a key event in the genesis of the lesions of atherosclerosis. Science. 180:1973;1332-1339.
7. Schwartz S., Campbell G., Campbell J. Replication of smooth muscle cells in vascular disease. Circ Res. 58:1986;427-444.
8. Schwartz S., deBlois D., O'Brien E. The intima. Soil for atherosclerosis and restenosis. Circ Res. 77:1995;445-465.
9. Abedi H., Zachary J. Signalling mechanisms in the regulation of vascular cell migration. Cardiovasc Res. 30:1995;544-556.
10. Weissberg P.L., Clesham G.J., Bennett M.R. Is vascular smooth-muscle cell-proliferation beneficial? Lancet. 347:1996;305-307.
11. Newby A.C., George S.J. Proliferation, migration, matrix turnover, and death of smooth-muscle cells in native coronary and vein graft atherosclerosis. Curr Opin Cardiol. 11:1996;574-582.
12. Orekhov A.N., Karpova I.I., Tertov V.V.et al. Cellular composition of atherosclerotic and uninvolved human aortic subendothelial intima: Light microscopic study of dissociated aortic cells. Am J Pathol. 115:1984;17-24.
13. Stary H.C. The sequence of cell and matrix changes in atherosclerotic lesions of coronary arteries in the first forty years of life. Eur Heart J. 11(Supple E):1990;3-19.
14. Kragel A.H., Reddy S.G., Wittes J.T., Roberts W.C. Morphometric analysis of the composition of atherosclerotic plaques in the four major epicardial coronary arteries in acute myocardial infarction and in sudden coronary death. Circulation. 80:1989;1747-1756.
15. Stary H., Chandler A., Dinsmore R.et al. A definition of advanced types of atherosclerotic lesions and a histological classification of atherosclerosis. A report from the Committee on Vascular Lesions of the Council on Atherosclerosis, American Heart Association. Arterioscler Thromb Vasc Biol. 15:1995;1512-1531.
16. Anitschkow N., Chalatow S. Uber experimentelle cholesterinsteatose und ihre bendeutung fur die enstehung einiger. Pathologischer prozess. Allg Pathol Anat. 24:1913;1-13.
17. Daley S., Klemp K., Guyton J., Rogers K. Cholesterol-fed and casein-fed rabbit models of atherosclerosis. Part 2: Differing morphological severity of atherogenesis despite matched plasma cholesterol levels. Arterioscler Thromb. 14:1994;105-114.
18. Faggiotto A., Ross R., Harker L. Studies of hypercholesterolaemia in the non-human primate. 1. Changes that lead to fatty streak formation. Arteriosclerosis. 4:1984;323-340.
19. Faggiotto A., Ross R. Studies of hypercholesterolaemia in the non-human primate. 2. Fatty streak conversion to fibrous plaque. Arteriosclerosis. 4:1984;341-356.
20. Masuda J., Ross R. Atherogenesis during low level hypercholesterolemia in the nonhuman primate. 1. Fatty streak formation. Arteriosclerosis. 10:1990;164-177.
21. Masuda J., Ross R. Atherogenesis during low level hypercholesterolemia in the nonhuman primate. 2. Fatty streak conversion to fibrous plaque. Arteriosclerosis. 10:1990;178-187.
22. Watanabe Y. Serial inbreeding of rabbits with hereditary hyperlipidemia (WHHL) rabbits. Atherosclerosis. 36:1980;261-268.
23. Buja L., Kita T., Goldstein J., Watanabe Y., Brown M. Cellular pathology of progressive atherosclerosis in the WHHL rabbit - an animal model of familial hypercholesterolemia. Arteriosclerosis. 3:1983;87-101.
24. Nakashima Y., Plump A., Raines E., Breslow J., Ross R. Apo-E-deficient mice develop lesions of all phases of atherosclerosis throughout the arterial tree. Arterioscler Thromb. 14:1994;133-140.
25. Thomas W., Kim D. Atherosclerosis as a hyperplastic and/or neoplastic process. Lab Invest. 48:1983;245-255.
26. Orekhov A.N., Andreeva E.R., Krushinski A.V.et al. Intimal cells and atherosclerosis: Relationship between the number of intimal cells and major manifestations of atherosclerosis in the human heart. Am J Pathol. 125:1986;402-415.
27. Velican C., Velican D. The precursors of coronary atherosclerotic plaques in subjects up to 40 years old. Atherosclerosis. 37:1980;33-46.
28. Aqel N.M., Ball R.Y., Waldmann H., Mitchinson M.J. Identification of macrophages and smooth muscle cells in human atherosclerosis using monoclonal antibodies. J Pathol. 146:1985;197-204.
29. Klurfeld D.M. Identification of foam cells in human atherosclerotic lesions as macrophages using monoclonal antibodies. Arch Pathol Lab Med. 109:1985;445-449.
30. Gown A.M., Tsukada T., Ross R. Human atherosclerosis: Immunocytochemical analysis of the cellular composition of human atherosclerotic lesions. Am J Pathol. 125:1986;191-207.
31. Poston R., Hussain I. The immunohistochemical heterogeneity of atheroma macrophages:comparison with lymphoid tissues suggest that recently blood-derived macrophages can be distinguished from longer-resident cells. J Histochem Cytochem. 41:1993;1503-1512.
32. Libby P., Geng Y., Aikawa M.et al. Macrophages and atherosclerotic plaque stability. Curr Opin Lipidol. 7:1996;330-335.
33. Nelken N., Coughlin S., Gordon D., Wilcox J. Monocyte chemoattractant protein-1 in human atheromatous plaques. J Clin Invest. 88:1991;1121-1127.
34. Berliner J.A., Territo M.C., Sevanian A.et al. Minimally modified low density lipoprotein stimulates monocyte endothelial interactions. J Clin Invest. 85:1990;1260-1266.
35. Gordon D., Reidy M., Benditt E., Schwartz S. Cell proliferation in human coronary arteries. Proc Natl Acad Sci USA. 87:1990;4600-4604.
36. Davies MJ, Woolf N. Atherosclerosis in ischaemic heart disease. The mechanisms. London: Science Press, 1990.
37. Ross R., Masuda J., Raines E.W.et al. Localization of PDGF-B protein in macrophages in all phases of atherogenesis. Science. 248:1990;1009-1012.
38. Shimokado K., Raines E., Madtes D.et al. A significant part of macrophage-derived growth factor consists of at least two forms of PDGF. Cell. 43:1985;277-286.
39. Higashiyama S., Abraham J., Klagsbrun M. Heparin-binding EGF-like growth factor stimulation of smooth muscle cell migration: dependence on interactions with cell surface heparan sulphate. J Cell Biol. 122:1993;933-940.
40. Yap A.S., Brieher W.M., Gumbiner B.M. Molecular and functional analysis of cadherin-based adherens junctions. Annu Rev Cell Dev Biol. 13:1997;119-146.
41. Navarro P., Ruco L., Dejana E. Differential localization of VE- and N-cadherins in human endothelial cells: VE-cadherin competes with N-cadherin for junctional localization. J Cell Biol. 140:1998;1475-1484.
42. Gilbertson-Beadling S.K., Fisher C. A potential role for N-cadherin in mediating endothelial cell-smooth muscle cell interactions in the rat vasculature. Lab Invest. 69:1993;203-209.
43. Pober J.S. Cytokine-mediated activation of vascular endothelium. Am J Pathol. 133:1988;426-433.
44. Kavanaugh W.M., Harsh G.R., Starksen N.F., Rocco C.M., Williams L.T. Transcriptional regulation of the A and B chain genes of platelet-derived growth factor in microvascular endothelial cells. J Biol Chem. 263:1988;1304-1309.
45. Koo E.W.Y., Gotlieb A.I. Endothelial stimulation of intimal cell proliferation in a porcine aortic organ culture. Am J Pathol. 134:1989;497-503.
46. Angelini G.D., Soyombo A.A., Newby A.C. Smooth muscle cell proliferation in response to injury in an organ culture of human saphenous vein. Eur J Vasc Surg. 5:1991;5-12.
47. George S.J., Williams A.W., Newby A.C. An essential role for platelet-derived growth factor in neointima formation in human saphenous vein in vitro. Atherosclerosis. 120:1996;227-240.
48. Davies M., Woolf N., Rowles P. Morphology of the endothelium over atherosclerotic plaques in human coronary arteries. Br Heart J. 60:1988;459-464.
49. Thompson W.D., McGuigan C.J., Snyder C., Keen G.A., Smith E.B. Mitogenic activity in human atherosclerotic lesions. Atherosclerosis. 66:1987;85-93.
50. Stirk C.M., Kochhar A., Smith E.B., Thompson W.D. Presence of growth stimulating fibrin degradation products containing fragment-E in human atherosclerotic plaques. Atherosclerosis. 103:1993;159-169.
51. Glagov S., Zarins C., Giddens D.P., Ku D.N. Hemodynamics and atherosclerosis. Arch Pathol Lab Med. 112:1988;1018-1031.
52. Angelini G.D., Bryan A.J., Williams H.M.J.et al. Timecourse of medial and intimal thickening in pig arteriovenous bypass grafts: relationship to endothelial injury and cholesterol accumulation. J Thorac Cardiovasc Surg. 103:1992;1093-1103.
53. Carmeliet P., Moons L., Lijnen R.et al. Urokinase-generated plasmin activates matrix metalloproteinases during aneurysm formation. Nat Genet. 17:1997;439-444.
54. Shiomi M., Ito T., Tsukada T., Yata T., Ueda M. Cell compositions of coronary and aortic atherosclerotic lesions in WHHL rabbits differ. An immunohistochemical study. Arterioscler Thromb. 14:1994;931-937.
55. Braverman A.C. Penetrating atherosclerotic ulcers of the aorta. Curr Opin Cardiol. 9:1994;591-597.
56. Bulkley B.H., Hutchins G.M. Accelerated atherosclerosis - a morphologic study of 97 saphenous vein coronary artery bypass grafts. Circulation. 55:1977;163-169.
57. Kaartinen M., Penttila A., Kovanen P. Mast cells of two types differing in neutral protease composition in the human aortic intima. Demonstration of tryptase- and tryptase/chymase-containing mast cells in normal intimas, fatty streaks, and the shoulder region of atheromas. Arterioscler Thromb. 14:1994;966-972.
58. Kaartinen M., Penttila A., Kovanen P. Mast cells in rupture-prone areas of human coronary atheromas produce and store TNF-α Circulation. 94:1996;2787-2792.
59. Walsh L., Trichieri G., Waldorf H., Whitaker D., Murphy G. Human dermal mast cells contain and release tumor necrosis factor α which induces endothelial leukocyte adhesion molecule 1. Proc Natl Acad Sci USA. 88:1991;4220-4224.
60. Wong G, Goeddel D. Tumor necrosis factor. In: Zembala M, Asherson G, editors. Human monocytes. San Diego, CA: Academic Press, 1989:195-215.
61. Chamley-Campbell J., Campbell G. What controls smooth muscle phenotype? Atherosclerosis. 40:1981;347-357.
62. Gabbiani G., Kocher O., Bloom W., Vanderkerchove J., Weber K. Actin expression in smooth muscle cells of rat aortic intimal thickening, human atheromatous plaque and cultured rat media. J Clin Invest. 73:1984;148-152.
63. Clowes A., Schwartz S. Significance of quiescent smooth muscle migration in the injured rat carotid artery. Circ Res. 56:1985;139-145.
64. Schwartz S., Reidy M., Clowes A. Kinetics of atherosclerosis. A stem cell model. Ann NY Acad Sci. 454:1985;292-304.
65. Clowes A.W., Reidy M.A., Clowes M.M. Kinetics of cellular proliferation after arterial injury. Smooth muscle growth in the absence of endothelium. Lab Invest. 49:1983;327-333.
66. Holifield B., Helgason T., Jemelka S.et al. Differentiated vascular myocytes: are they involved in neointimal formation? J Clin Invest. 97:1996;814-825.
67. Seidel C. Cellular heterogeneity of the vascular tunica media. Implications for vessel wall repair. Arterioscler Thromb Vasc Biol. 17:1997;1868-1871.
68. Frid M.G., Dempsey E.C., Durmowitcz A.G., Stenmark K.R. Smooth muscle cell heterogeneity in pulmonary and systemic vessels: Importance in vascular disease. Arterioscler Thromb Vasc Biol. 17:1997;1203-1209.
69. Kirschenlohr H.L., Metcalfe J.C., Weissberg P.L., Grainger D.J. Proliferation of human aortic vascular smooth muscle cells in culture is modulated by active TGF-beta. Cardiovasc Res. 29:1995;848-855.
70. Kocher O., Gabbiani G. Cytoskeletal features of normal and atheromatous human arterial smooth muscle cells. Hum Pathol. 17:1984;875-880.
71. Wilcox J.N., Smith K.M., Williams L.T., Schwartz S.M., Gordon D. Platelet-derived growth factor mRNA detection in human atherosclerotic plaques by in situ hybridization. J Clin Invest. 82:1988;1134-1143.
72. Glukhova M., Kabakov A., Frid M. Modulation of human aorta smooth muscle cell phenotype: a study of muscle-specific variants of vinculin, caldesmon and actin expression. Proc Nat Acad Sci USA. 85:1988;9542-9546.
73. Shi Y., O'Brien J.et al. Adventitial myofibroblasts contribute to neointimal formation in injured porcine coronary arteries. Circulation. 94:1996;1655-1664.
74. Wilcox J., Scott N. Potential role of the adventitia in arteritis and atherosclerosis. Int J Cardiol. 54:1996;S21-S35.
75. Shi Y., O'Brien J.E., Mannion J.D.et al. Remodeling of autologous saphenous vein grafts - The role of perivascular myofibroblasts. Circulation. 95:1997;2684-2693.
76. Benditt E.P., Benditt J.M. Evidence for a monoclonal origin of human atherosclerotic plaques. Proc Natl Acad Sci USA. 70:1973;1753-1756.
77. Murry C., Gipaya C., Bartosek T., Benditt E., Schwartz S. Monoclonality of smooth muscle cells in human atherosclerosis. Am J Pathol. 151:1997;697-705.
78. Penn A., Garte S.J., Warren L., Nesta D., Mindich B. Transforming gene in human atherosclerotic plaque DNA. Proc Natl Acad Sci USA. 83:1986;7951-7955.
79. Parkes J.L., Cardell R.R., Hubbard F.C.et al. Cultured human atherosclerotic plaque smooth muscle cells retain transforming potential and display enhanced expression of the myc protooncogene. Am J Pathol. 138:1991;765-775.
80. Bennett M.R., Evan G.I., Schwartz S.M. Apoptosis of human vascular smooth muscle cells derived from normal vessels and coronary atherosclerotic plaques. J Clin Invest. 95:1995;2266-2274.
81. Moss N., Benditt E. Human atherosclerotic plaque cells and leiomyoma cells. Am J Pathol. 78:1975;175-190.
82. Newby A.C., George S.J. Proposed roles for growth factors in mediating smooth muscle proliferation in vascular pathologies. Cardiovasc Res. 27:1993;1173-1183.
83. Newby A. Molecular and cell biology of native coronary and vein-graft atherosclerosis: regulation of plaque stability and vessel-wall remodelling by growth factors and cell-extracellular matrix interactions. Coron Artery Dis. 8:1997;213-224.
84. Molloy C., Pawlowski J., Taylor D.et al. Thrombin receptor activation elicits rapid tyrosine phosphorylation and stimulation of the Raf-1/MAP kinase pathway preceding delayed mitogenesis in cultured rat aortic smooth muscle cells. Evidence for an obligate autocrine mechanism promoting cell proliferation induced by G protein-coupled receptor agonists. J Clin Invest. 97:1996;1173-1183.
85. Malarkey K., McLees A., Paul A., Gould G., Plevin R. The role of protein kinase C in activation and termination of mitogen-activated protein kinase activity in angiotensin II-stimulated rat aortic smooth-muscle cells. Cell Signal. 8:1996;123-129.
86. Polyak K. Negative regulation of cell growth by TGFβ Biochim Biophys Acta. 1242:1996;185-199.
87. Heim M.H. The Jak-Stat pathway-specific signal transduction from the cell membrane to the nucleus. Eur J Clin Invest. 26:1996;1-12.
88. McCaffrey T., Consigli S., Du B.et al. Decreased type II/type I TGF-β receptor ratio in cells derived from human atherosclerotic lesions. Conversion from an antiproliferative to profibrotic response to TGF-β J Clin Invest. 96:1995;2667-2675.
89. Björkerud S., Björkerud B. Lipoproteins are major primary mitogens and growth promoters for human arterial smooth muscle cells and lung fibroblasts in vitro. Arterioscler Thromb. 14:1994;288-298.
90. Libby P., Miao P., Ordovas J.M., Schaefer E.J. Lipoproteins increase growth of mitogen stimulated arterial smooth muscle cells. J Cell Physiol. 124:1985;1-8.
91. Björkerud B., Björkerud S. Contrary effects of lightly and strongly oxidised LDL with potent promotion of growth versus apoptosis on arterial smooth muscle cells, macrophages and fibroblasts. Arterioscler Thromb Vasc Biol. 16:1996;416-424.
92. Barrett T.B., Benditt E.P. Platelet-derived growth-factor gene-expression in human atherosclerotic plaques and normal artery wall. Proc Natl Acad Sci USA. 85:1988;2810-2814.
93. Libby P., Warner S.J.C., Salomon R.N., Birinyi L.K. Production of platelet-derived growth factor-like mitogen by smooth muscle cells from human atheroma. N Engl J Med. 318:1988;1493-1498.
94. Murry C., Bartosek T., Giachelli C., Alpers C., Schwartz S. Platelet-derived growth factor-A mRNA expression in fetal, normal adult, and atherosclerotic human aortas: Analysis by competitive polymerase chain reaction. Circulation. 93:1996;1095-1106.
95. Rubin K., Tingström A., Hansson G.K.et al. Induction of B-type receptors for platelet-derived growth factor in vascular inflammation: possible implications for development of vascular proliferative lesions. Lancet. 1:1988;1353-1356.
96. Wilson V., Ward J., Burnand K., Thomas C. Up-regulation of IGF-1 and collagen-1 messenger-RNA in human atherosclerotic tissue is not accompanied by changes in type-1 IGF receptor or collagen messenger-RNA - an in-situ hybridization study. Coron Artery Dis. 7:1996;569-572.
97. Nikol S., Isner J.M., Pickering J.G.et al. Expression of transforming growth factor-β1 is increased in human vascular restenosis lesions. J Clin Invest. 90:1992;1582-1592.
98. Liau G., Winkles J.A., Cannon M.S., Kuo L., Chilian W.M. Dietary-induced atherosclerotic lesions have increased levels of acidic FGF messenger-RNA and altered cytoskeletal and extracellular-matrix messenger-RNA expression. J Vasc Res. 30:1993;327-332.
99. Hughes S.E. Localization and differential expression of the fibroblast growth-factor receptor (FGFR) multigene family in normal and atherosclerotic human arteries. Cardiovasc Res. 32:1996;557-569.
100. McNamara C., Sarembock I., Gimple L.et al. Thrombin stimulates proliferation of cultured rat aortic smooth muscle cells by a proteolytically activated receptor. J Clin Invest. 91:1993;94-98.
101. Pasche B., Swedenborg J., Hedin U., Olsson P., Ljungqvist A. Thrombin-inhibitory capacity of the injured vessel wall. Thromb Res. 62:1991;531-544.
102. Nelken N., Soifer S., O'Keefe J.et al. Thrombin receptor expression in normal and atherosclerotic human arteries. J Clin Invest. 90:1992;1614-1621.
103. Kowala M., Rose P., Stein P.et al. Selective blockage of the endothelin subtype-A receptor decreases early atherosclerosis in hamsters fed cholesterol. Am J Pathol. 146:1995;819-826.
104. Ferns G.A.A., Raines E.W., Sprugel K.H.et al. Inhibition of neointimal smooth muscle accumulation after angioplasty by an antibody to PDGF. Science. 253:1991;1129-1132.
105. Lindner V., Reidy M.A. Proliferation of smooth muscle cells after vascular injury is inhibited by an antibody against basic fibroblast growth factor. Proc Natl Acad Sci USA. 88:1991;3739-3743.
106. Rutherford C., Martin W., Salame M.et al. Substantial inhibition of neo-intimal response to balloon injury in the rat carotid artery using a combination of antibodies to platelet-derived growth factor-BB and basic fibroblast growth factor. Atherosclerosis. 130:1997;45-51.
107. Wolf Y., Rasmussen L., Ruoslahti E. Antibodies against transforming growth factor-1 suppress intimal hyperplasia in a rat model. J Clin Invest. 93:1994;1172-1178.
108. Fennessy P.A., Campbell J.H., Campbell G.R. An angiotensin-converting enzyme-inhibitor, perindopril, prevents progression of preformed atherosclerotic lesions in the cholesterol-fed rabbit. Clin Sci. 87:1994;685-691.
109. 1 receptor antagonist: effects on smooth muscle cell migration and proliferation after balloon catheter injury. Am J Pathol. 139:1991;1291-1296.
110. Israel D.H., Adams P.C., Stein B., Chesebro J.H., Fuster V. Anti-thrombotic therapy in the coronary vein graft patient. Clin Cardiol. 14:1991;283-295.
111. Fingerle J., Kraft T. The induction of smooth muscle cell proliferation in vitro using an organ culture system. Int Angiol. 6:1987;65-72.
112. Soyombo A.A., Angelini G.D., Bryan A.J., Newby A.C. Surgical preparation induces injury and promotes smooth muscle cell proliferation in a culture of human saphenous vein. Cardiovasc Res. 27:1993;1961-1967.
113. Fingerle J., Au Y.P.T., Clowes A.W., Reidy M.A. Intimal lesion formation in rat carotid arteries after endothelial denudation in absence of medial injury. Arteriosclerosis. 10:1990;1082-1087.
114. Rifkin D.B., Moscatelli D. Recent developments in the cell biology of basic fibroblast growth factor. J Cell Biol. 109:1989;1-6.
115. Southgate K.M., Davies M., Booth R.F.G., Newby A.C. Involvement of extracellular matrix degrading metalloproteinases in rabbit aortic smooth muscle cell proliferation. Biochem J. 288:1992;93-99.
116. Clowes A.W., Clowes M.M. Kinetics of cellular proliferation after arterial injury. IV. Heparin inhibits rat smooth muscle mitogenesis and migration. Circ Res. 58:1986;839-845.
117. Campbell J.H., Campbell G.R. Endothelial cell influences on vascular smooth muscle phenotype. Annu Rev Physiol. 48:1986;295-306.
118. Au Y.P.T., Dobrowolska G., Morris D.R., Clowes A.W. Heparin decreases activator protein-1 binding to DNA in part by posttranslational modification of Jun B. Circ Res. 75:1994;15-22.
119. Wight T., Hascall V. Proteoglycans in primate arteries: III. Characterisation of the proteoglycans synthesized by arterial smooth muscle cells in culture. J Cell Biol. 96:1983;167-176.
120. Kenagy R.D., Nikarri S.T., Welgus H.G., Clowes A.W. Heparin inhibits the induction of three matrix metalloproteinases (stromelysin, 92-kDa gelatinase, and collagenase) in primate arterial smooth muscle cells. J Clin Invest. 93:1994;1987-1993.
121. Clowes A., Clowes M.M., Kirkman T.R.et al. Heparin inhibits the expression of tissue-type plasminogen activator by smooth muscle cells in injured rat carotid artery. Circ Res. 70:1992;1128-1136.
122. Hedin U., Bottger B.A., Forsberg E., Johansson S., Thyberg J. Diverse effects of fibronectin and laminin on phenotypic properties of cultured smooth muscle cells. J Cell Biol. 107:1988;307-319.
123. Hedin U., Bottger B.A., Lutham J., Johansson S., Thyberg J. A substrate of the cell attachment sequence of fibronectin (Arg-Gly-Asp-Ser) is sufficient to promote transition of arterial smooth muscle cells from a contractile to a synthetic phenotype. Dev Biol. 133:1989;489-501.
124. Thyberg J., Hedin U., Sjölund M., Palmberg L., Bottger B.A. Regulation of differentiated properties and proliferation of arterial smooth muscle cells. Arteriosclerosis. 10:1990;966-990.
125. Newby A.C., Fabunmi R.P., George S.J.et al. Neointimal fibrosis in vascular pathologies: role of growth factors and metalloproteinases in vascular smooth muscle proliferation. Exp Nephrol. 3:1995;108-113.
126. Koyama H., Raines E.W., Bornfeldt K.E., Roberts J.M., Ross R. Fibrillar collagen inhibits arterial smooth muscle proliferation through regulation of CDK2 inhibitors. Cell. 87:1996;1069-1078.
127. Galis Z.S., Muszynski M., Sukhova G.K.et al. Cytokine-stimulated human vascular smooth muscle cells synthesize a complement of extracellular enzymes required for extracellular matrix degradation. Circ Res. 75:1994;181-189.
128. Sato H., Takino T., Okada Y.et al. A matrix metalloproteinase expressed on the surface of invasive tumour cells. Nature. 370:1994;61-65.
129. Galis Z.S., Kranshöfer R., Fenton J.W., Libby P. Thrombin promotes activation of matrix metalloproteinase-2 produced by cultured vascular cells. Arterioscler Thromb Vasc Biol. 17:1997;483-489.
130. Rajagopalan S., Meng X.P., Ramasamy S., Harrison D.G., Galis Z.S. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. J Clin Invest. 98:1996;2572-2579.
131. Fabunmi R.P., Baker A.H., Murray E.J., Booth R.F.G., Newby A.C. Divergent regulation by growth factors and cytokines of 95-kDa and 72-kDa gelatinases and tissue inhibitors of metalloproteinases-1, -2 and -3 in rabbit aortic smooth muscle cells. Biochem J. 315:1996;335-342.
132. Bendeck M.P., Zempo N., Clowes A.W., Gelardy R.E., Reidy M.A. Smooth muscle cell migration and matrix metalloproteinase expression after arterial injury in the rat. Circ Res. 75:1994;539-545.
133. Zempo N., Kenagy R.D., Au T.et al. Matrix metalloproteinases of vascular wall cells are increased in balloon-injured rat carotid artery. J Vasc Surg. 20:1994;209-217.
134. Southgate K.M., Banning A.P., Thurston V.J.et al. Upregulation of basement-membrane-degrading metalloproteinase secretion following balloon angioplasty of pig carotid arteries. Circ Res. 79:1996;1177-1187.
135. George S.J., Zaltsman A.B., Newby A.C. Surgical preparative injury and neointima formation increase MMP-9 expression and MMP-2 activation in human saphenous vein. Cardiovasc Res. 33:1997;447-459.
136. Zempo N., Koyama N., Kenagy R., Lea H., Clowes A. Regulation of vascular smooth muscle cell migration and proliferation in vitro and injured rat arteries by a synthetic matrix metalloproteinase inhibitor. Arterioscler Thromb Vasc Biol. 16:1996;28-33.
137. Bendeck M.P., Irvin C., Reidy M.A. Inhibition of matrix metalloproteinase activity inhibits smooth muscle cell migration but not neointimal thickening after arterial injury. Circ Res. 78:1996;38-43.
138. Forough R., Koyama M., Hasenstab D.et al. Overexpression of tissue inhibitor of metalloproteinase-1 inhibits vascular smooth muscle cell functions in vitro and in vivo. Circ Res. 79:1996;812-820.
139. George S., Johnson J., Angelini G., Newby A., Baker A. Adenovirus-mediated gene transfer of the human TIMP-1 gene inhibits smooth muscle cell migration and neointimal formation in human saphenous vein. Hum Gene Ther. 9:1998;867-877.
140. Bartlett M.R., Cowden W.B., Parish C.R. Differential effects of the antiinflammatory compounds heparin, mannose-6-phosphate, and castanospermine on degradation of the vascular basement membrane by leukocytes, endothelial cells and platelets. J Leukocyte Biol. 57:1995;207-213.
141. Bartlett M.R., Underwood P.A., Parish C.R. Comparative-analysis of the ability of leukocytes, endothelial-cells and platelets to degrade the subendothelial basement-membrane - Evidence for cytokine dependence and detection of a novel sulfatase. Immunol Cell Biol. 73:1995;113-124.
142. Chapman H.A., Reise R.J., Shi G.P. Emerging roles for cysteine proteases in human biology. Annu Rev Physiol. 59:1997;63-88.
143. Millichip M.I., Dallas D.J., Wu E.X., Dale S., McKie N. The metallo-disintegrin ADAM10 (MADM) from bovine kidney has type IV collagenase activity in vitro. Biochem Biophys Res Commun. 245:1998;594-598.
144. Henney A.M., Wakely P.R., Davies M.J.et al. Localization of stromelysin gene expression in atherosclerotic plaques by in situ hybridization. Proc Natl Acad Sci USA. 88:1991;8154-8158.
145. Galis Z.S., Suhova G.K., Lark M.W., Libby P. Increased expression of matrix metalloproteinases and matrix degrading activity in vulnerable regions of human atherosclerotic plaques. J Clin Invest. 94:1994;2493-2503.
146. Galis Z.S., Sukhova G.K., Kranshöfer R., Clark S., Libby P. Macrophage foam cells from experimental atheroma constitutively express matrix-degrading proteases. Proc Natl Acad Sci USA. 92:1995;402-406.
147. Nikkari S.T., O'Brien K.D., Ferguson M.et al. Interstitial collagenase (MMP-1) expression in human carotid atherosclerosis. Circulation. 92:1995;1393-1398.
148. Li Z., Li L., Zielke R.et al. Increased expression of 72-kD type IV collagenase (MMP-2) in human aortic atherosclerotic lesions. Am J Pathol. 148:1996;121-128.
149. Zaltsman A.B., Newby A.C. Increased secretion of gelatinases A and B from the aortas of cholesterol fed rabbits: relationship to lesion severity. Atherosclerosis. 130:1997;61-70.
150. Carmeliet P., Moons L., Dewerchin M.et al. Receptor-independent role of urokinase-type plasminogen activator in pericellular plasmin and matrix metalloproteinase proteolysis during vascular wound healing in mice. J Cell Biol. 140:1998;233-245.
151. van Leeuwen R. Extracellular proteolysis and the migrating vascular smooth muscle cell. Fibrinolysis. 10:1996;59-74.
152. Bornfeldt K., Raines E., Nakano T.et al. Insulin-like growth factor-1 and platelet-derived growth factor-BB induce directed migration of human arterial smooth muscle cells via signalling pathways that are distinct from those of proliferation. J Clin Invest. 93:1994;1266-1274.
153. Ross R. Cellular interactions, growth factors, and atherogenesis. Prev Noninvasive Ther Atheroscler. 21:1990;53-58.
154. Koyama N., Morisaki N., Saito Y., Yoshida S. Regulatory effects of PDGF-AA homodimer on migration of vascular smooth muscle cells. J Biol Chem. 267:1992;22806-22812.
155. Koyama N., Hart C.E., Clowes A.W. Different effects of platelet-derived growth factor-a and b receptors for the migration and proliferation of cultured baboon smooth muscle cells. Circ Res. 75:1994;682-691.
156. Pauly R.R., Bilato C., Sollott S.J.et al. Role of calcium calmodulin dependent protein kinase-II in the regulation of vascular smooth muscle cell migration. Circulation. 91:1995;1107-1115.
157. Bilato C., Pauly R.R., Melillo G.et al. Intracellular signaling pathways required for rat vascular smooth muscle cell migration - Interactions between basic fibroblast growth factor and platelet-derived growth factor. J Clin Invest. 96:1995;1905-1915.
158. Olson N.E., Chao S., Lindner V., Reidy M.A. Intimal smooth muscle cell proliferation after balloon catheter injury: The role of basic fibroblast growth factor. Am J Pathol. 140:1992;1017-1023.
159. Yabkowitz R., Mansfield P., Ryan U., Suchard S. Trombospondin mediates migration and potentiates platelet-derived growth factor-dependent migration of calf pulmonary artery smooth muscle cells. J Cell Physiol. 157:1993;24-32.
160. Kishi J.-I., Hayakawa T. Synthesis of latent collagenase and collagenase inhibitor by bovine aortic medial explants and cultured medial smooth muscle cells. Connect Tissue Res. 19:1989;63-76.
161. Casscells W. Migration of smooth muscle and endothelial cells. Critical events in restenosis. Circulation. 86:1992;723-729.
162. Reidy M., Irvin C., Lindner V. Migration of arterial wall cells. Expression of plasminogen activators and inhibitors in injured rat arteries. Circ Res. 78:1996;405-414.
163. Pauly R.R., Passaniti A., Bilato C.et al. Migration of cultured vascular smooth muscle cells through a basement membrane barrier requires type IV collagenase activity and is inhibited by cellular differentiation. Circ Res. 75:1994;41-45.
164. Baker A., Zaltsman A., George S., Newby A. Divergent effects of tissue inhibitor of metalloproteinase-1, -2, or -3 overexpression on rat vascular smooth muscle cell invasion, proliferation, and death in vitro. J Clin Invest. 101:1998;1478-1487.
165. Kenagy R., Hart C., Stetler-Stevenson W., Clowes A. Primate smooth muscle cell migration from aortic explants is mediated by endogenous platelet-derived growth factor and basic fibroblast growth factor acting through matrix metalloproteinases 2 and 9. Circulation. 96:1997;3555-3560.
166. Clowes A.W., Clowes M.M., Reidy M.A., Belin D. Smooth muscle cells express urokinase during mitogenesis and tissue-type plasminogen activator during migration in injured rat carotid artery. Circ Res. 67:1990;61-67.
167. Jackson C.L., Reidy M.A. The role of plasminogen activation in smooth muscle cell migration after arterial injury. Ann NY Acad Sci. 667:1992;141-150.
168. Jackson C.L., Raines E.W., Ross R., Reidy M.A. Role of endogenous platelet-derived growth factor in arterial smooth muscle cell migration after balloon catheter injury. Arterioscler Thromb. 1993:1993;13.
169. Carmeliet P., Moons L., Lijnen R.et al. Inhibitory role of plasminogen activator inhibitor-1 in arterial wound healing and neointima formation. A gene targeting and gene transfer study in mice. Circulation. 96:1997;3180-3191.
170. Ang A.H., Tachas G., Campbell J.H., Bateman J.F., Campbell G.R. Collagen synthesis by cultured rabbit aortic smooth muscle cells. Biochem J. 265:1990;461-469.
171. Thyberg J. Differentiated properties and proliferation of arterial smooth muscle cells in culture. Int Rev Cytol. 169:1996;183-265.
172. Savani R., Wang C., Yang B.et al. Migration of bovine aortic smooth muscle cells after wounding injury - the role of hyaluronan and rhamm. J Clin Invest. 95:1995;1158-1168.
173. Wight T. The extracellular matrix and atherosclerosis. Curr Opin Lipidol. 6:1995;326-334.
174. Thyberg J., Blomgren K., Roy J., Tran P.K., Hedin U. Phenotypic modulation of smooth muscle cells after arterial injury is associated with changes in the distribution of laminin and fibronectin. J Histochem Cytochem. 45:1997;837-846.
175. Koyama N., Koshikawa T., Morisaki N., Saito Y., Yoshida S. Secretion of a potent new migration factor for smooth muscle cells (SMC) by cultured SMC. Atherosclerosis. 86:1991;219-226.
176. DiMilla P., Stone J., Quinn J., Albelda S., Lauffenburger D. Maximal migration of human smooth muscle cells on fibronectin and type IV collagen occurs at an intermediate attachment strength. J Cell Biol. 122:1993;729-737.
177. Liaw L., Slinner M., Raines E.et al. The adhesive and migratory effects
178. Skinner M.P., Raines E.W., Ross R. Dynamic expression of alpha-1-beta-1 and alpha-2-beta-1 integrin receptors by human vascular smooth muscle cells - - alpha-2-beta-1 integrin is required for chemotaxis across type-I collagen coated membranes. Am J Pathol. 145:1994;1070-1081.
179. Naito M., Hayasi T., Funaki C.et al. Vitronectin-induced haptotaxis of vascular smooth muscle cells in vitro. Exp Cell Res. 194:1991;154-156.
180. Brown E., Landgren C., Nordt T., Fujii S. Stimulation of migration of human aortic smooth muscle cells by vitronectin: implications for atherosclerosis. Cardiovasc Res. 28:1994;1815-1820.
181. Wight T. Cell biology of arterial proteoglycans. Arteriosclerosis. 9:1989;1-20.
182. Shekhonin B., Domogatsky S., Idelson G., Koteliansky V., Rukosuerm V.S. Relative distribution of fibronectin and type I, III, IV, V collagens in normal and atherosclerotic intima of human arteries. Atherosclerosis. 67:1987;9-16.
183. Murata K., Motoyama T., Kotake C. Collagen types in various layers of the human aorta and their changes with the atherosclerotic process. Atherosclerosis. 60:1986;251-262.
184. Rekhter M., Zhang K., Narayanan A.et al. Type-1 collagen gene-expression in human atherosclerosis - localization to specific plaque regions. Am J Pathol. 143:1993;1634-1648.
185. Rekhter M., Gordon D. Cell proliferation and collagen synthesis are two independent events in human atherosclerotic plaques. J Vasc Res. 31:1994;280-286.
186. Roberts A., Sporn M., Assoian R.et al. Transforming growth factor type beta: rapid induction of fibrosis and angiogenesis in vivo and stimulation of collagen formation in vitro. Proc Natl Acad Sci USA. 83:1986;4167-4171.
187. Ignoltz R., Massague J. Transforming growth factor-beta stimulates the expression of fibronectin and collagen and their incorporation into the extracellular matrix. J Biol Chem. 261:1986;4337-4345.
188. Bendeck M., Regenass S., Tom W.et al. Differential expression of α1 type VIII collagen in injured platelet-derived growth factor-BB-stimulated rat carotid arteries. Circ Res. 79:1996;524-531.
189. Shanahan C.M., Weissberg P.L., Metcalfe J.C. Isolation of gene markers of differentiated and proliferating vascular smooth muscle cells. Circ Res. 73:1993;193-204.
190. Giachelli C.M., Bae N., Almeida M.et al. Osteopontin is elevated during neointima formation in rat arteries and is a novel component of human atherosclerotic plaques. J Clin Invest. 92:1993;1686-1696.
191. Majack R.A., Cook S.C., Bornstein P. Control of smooth muscle cell growth by components of the extracellular matrix: autocrine role for thrombospondin. Proc Natl Acad Sci USA. 83:1986;9050-9054.
192. Matsuno H., Stassen J., Vermylen J., Deckmyn H. Inhibition of integrin function by a cyclic RGD-containing peptide prevents neointima formation. Circulation. 90:1994;2203-2206.
193. Srivatsa S., Fitzpatrick L., Tsao P.et al. Selective αvβ3 integrin blockade potently limits neointimal hyperplasia and lumen stenosis following deep coronary arterial stent injury: evidence for the functional importance of integrin αvβ3 and osteopontin expression during neointima formation. Cardiovasc Res. 36:1997;408-428.
194. Lendon C.L., Davies M.J., Born G.V.R., Richardson P.D. Atherosclerotic plaque caps are locally weakened when macrophage density is increased. Atherosclerosis. 87:1991;87-91.
195. Mann J.M., Davies M.J. Vulnerable plaque. Relation of characteristics to degree of stenosis in human coronary arteries. Circulation. 94:1996;928-931.
196. Libby P. Molecular basis of the acute coronary syndromes. Circulation. 91:1995;2844-2850.
197. Libby P., Sukhova G., Lee R.T., Galis Z.S. Cytokines regulate vascular functions related to stability of the atherosclerotic plaque. J Cardiovasc Pharmacol. 25:1995;S9-S12.
198. Lindner V., Majack R.A., Reidy M.A. Basic fibroblast growth factor stimulates endothelial regrowth and proliferation in denuded arteries. J Clin Invest. 85:1990;2004-2008.
199. Kerr L., Olashaw N., Matrisian L. Transforming growth factor β1 and cAMP inhibit transcription of epidermal growth factor- and oncogene-induced transin RNA. J Biol Chem. 263:1988;16999-17005.
200. Motoyama Y., Seki J., Katoh Y., Nishio M., Yoshida K. Effect of TFC-612, a 7-thia prostaglandin E1 derivative, on intimal thickening after endothelial injury with balloon catheter in rats. Atherosclerosis. 108:1994;159-165.
201. Garg U.C., Hassid A. Nitric oxide-generating vasodilators inhibit mitogenesis and proliferation of BALB/C 3T3 fibroblasts by a cyclic GMP-dependent mechanism. Biochem Biophys Res Commun. 171:1990;474-479.
202. Kariya K., Kawahara Y., Araki S.-I., Fukuzaki H., Takai Y. Antiproliferative action of cyclic GMP-elevating vasodilators in cultured rabbit aortic smooth muscle cells. Atherosclerosis. 80:1989;143-147.
203. 2+ mobilization by cAMP and cGMP in rabbit aortic smooth muscle cells. Biochem J. 288:1992;527-532.
204. Hansson G.K., Hellstrand M., Rymo L., Rubbia L., Gabbiani G. Interferon-gamma inhibits both proliferation and expression of differentiation specific alpha-smooth muscle actin in arterial smooth muscle cells. J Exp Med. 170:1989;1595-1608.
205. Hansson G.K., Holm J. Interferon-γ inhibits arterial stenosis after injury. Circulation. 84:1991;1266-1272.
206. Laitinen M., Zachary I., Breier G.et al. VEGF gene transfer reduces intimal thickening via increased production of nitric oxide in carotid arteries. Hum Gene Ther. 8:1997;1737-1744.
207. Graves L.M., Bornfeldt K.E., Raines E.W.et al. Protein kinase A antagonizes platelet-derived growth factor signaling by mitogen-activated protein kinase in human arterial smooth muscle cells. Proc Natl Acad Sci USA. 90:1993;10300-10304.
208. L'Allemain G., Lavoie J., Rivard N., Baldin V., Pouyssegur J. Cyclin D1 expression is a major target of the cAMP-induced inhibition of cell cycle entry in fibroblasts. Oncogene. 14:1997;1981-1990.
209. Bennett M.R., Littlewood T.D., Hancock D.C., Evan G.I., Newby A.C. Down-regulation of the c-myc proto-oncogene in arrest of rat aortic vascular smooth muscle cell proliferation - different effects of mitogen withdrawal, heparin, interferon-gamma and cyclic nucleotide analogues. Biochem J. 302:1994;701-708.
210. Bennett M.R., Evan G.I., Newby A.C. Deregulated expression of the c-myc oncogene abolishes inhibition of proliferation of rat vascular smooth muscle cells by serum reduction, interferon-γ, heparin and cyclic nucleotide analogues and induces apoptosis. Circ Res. 74:1994;525-536.
211. Hansson G., Stemme S., Geng Y., Holm J. Can immunocompetent cells and their cytokines play a role in atherogenesis? Nouv Rev Fr Hematol. 34:1992;543-546.
212. Palinski W., Miller E., Witztum J. Immunization of low-density-lipoprotein (LDL) receptor deficient rabbits with homologous malondialdehyde-modified LDL reduces atherogenesis. Proc Natl Acad Sci USA. 92:1995;821-825.
213. Ameli S., Hultgardhnilsson A., Regnstrom J.et al. Effect of immunization with homologous LDL and oxidized LDL on early atherosclerosis in hypercholesterolemic rabbits. Arterioscler Thromb Vasc Biol. 16:1996;1074-1079.
214. Bennett M., Macdonald K., Chan S., Boyle J., Weissberg P. Cooperative interaction between RB and p53 regulate cell proliferation, cell senescence, and apoptosis in human vascular smooth muscle cells from atherosclerosis plaques. Circ Res. 82:1998;704-712.
215. Isner J.M., Kearney M., Bortman S., Passeri J. Apoptosis in human atherosclerosis and restenosis. Circulation. 91:1995;2703-2711.
216. Han D.K.M., Haudenschild C.C., Hong M.K.et al. Evidence for apoptosis in human atherogenesis and in a rat vascular injury model. Am J Pathol. 147:1995;267-277.
217. Geng Y.J., Libby P. Evidence for apoptosis in advanced human atheroma - colocalization with interleukin-1-beta-converting enzyme. Am J Pathol. 147:1995;251-266.
218. Kockx M.M., Muhring J., Bortier H., Demeyer G.R.Y., Jacob W. Biotin-conjugated or digoxigenin-conjugated nucleotides bind to matrix vesicles in atherosclerotic plaques. Am J Pathol. 148:1996;1771-1777.
219. Kockx M.M., Muhring J., Knaapen M.W.M., deMeyer G.R.Y. RNA synthesis and splicing interferes with DNA in situ end labeling techniques used to detect apoptosis. Am J Pathol. 152:1998;885-888.
220. Yu H., Gallagher A.M., Garfin P.M., Printz M.P. Prostacyclin release by rat cardiac fibroblasts - Inhibition of collagen expression. Hypertension. 30:1997;1047-1053.
221. Kolpakov V., Gordon D., Kulik T. Nitric oxide-generating compounds inhibit total protein and collagen-synthesis in cultured vascular smooth muscle cells. Circ Res. 76:1995;305-309.